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Historical Biogeography and Diversification of Truffles in the Tuberaceae and Their Newly Identified Southern Hemisphere Sister Lineage Public Deposited

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  • Truffles have evolved from epigeous (aboveground) ancestors in nearly every major lineage of fleshy fungi. Because accelerated rates of morphological evolution accompany the transition to the truffle form, closely related epigeous ancestors remain unknown for most truffle lineages. This is the case for the quintessential truffle genus Tuber, which includes species with socio-economic importance and esteemed culinary attributes. Ecologically, Tuber spp. form obligate mycorrhizal symbioses with diverse species of plant hosts including pines, oaks, poplars, orchids, and commercially important trees such as hazelnut and pecan. Unfortunately, limited geographic sampling and inconclusive phylogenetic relationships have obscured our understanding of their origin, biogeography, and diversification. To address this problem, we present a global sampling of Tuberaceae based on DNA sequence data from four loci for phylogenetic inference and molecular dating. Our well-resolved Tuberaceae phylogeny shows high levels of regional and continental endemism. We also identify a previously unknown epigeous member of the Tuberaceae - the South American cup-fungus Nothojafnea thaxteri (E.K. Cash) Gamundi. Phylogenetic resolution was further improved through the inclusion of a previously unrecognized Southern hemisphere sister group of the Tuberaceae. This morphologically diverse assemblage of species includes truffle (e.g. Gymnohydnotrya spp.) and non-truffle forms that are endemic to Australia and South America. Southern hemisphere taxa appear to have diverged more recently than the Northern hemisphere lineages. Our analysis of the Tuberaceae suggests that Tuber evolved from an epigeous ancestor. Molecular dating estimates Tuberaceae divergence in the late Jurassic (~156 million years ago), with subsequent radiations in the Cretaceous and Paleogene. Intra-continental diversification, limited long-distance dispersal, and ecological adaptations help to explain patterns of truffle evolution and biodiversity.
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  • Bonito G, Smith ME, Nowak M, Healy RA, Guevara G, et al. (2013) Historical Biogeography and Diversification of Truffles in the Tuberaceae and Their Newly Identified Southern Hemisphere Sister Lineage. PLoS ONE 8(1): e52765. doi:10.1371/journal.pone.0052765
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  • This research was supported through NSF award #0641297, REVSYS: Phylogenetic and Revisionary Systematics of North American Truffles (Tuber). Support was also provided by the Friends of the Farlow, which enabled the senior author to conduct research at the Farlow Herbarium. M.E.S. participated via a postdoctoral fellowship from Harvard University Herbaria. D.H.P. received funding from the David Rockefeller Center for Latin American Studies at Harvard University that supported field work in collaboration with M.E.S. Collections and microscopy were enabled by a grant from the Iowa Science Foundation to R.H. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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